Metabolism of nitrogen and sulfur in ectosymbiotic bacteria of marine nematodes (Nematoda, Stilbonematinae)

Hentschel, Ute; Berger, Eldie; Bright, Monika; Felbeck, Horst; Ott, Jörg

doi:10.3354/meps183149

Cited by 46 publications

(50 citation statements)

References 14 publications

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“…The vertical profiles of GAM660-detected rRNA, and GAM660 target cells showed no stratification as might be expected for aerobic chemoautotrophic organisms. However, nitrate respiration has been demonstrated in several endosymbionts, for example, from Solemya reidi (71), Riftia pachyptila (27), and Lucinoma aequizonata (26), as well as in the ectosymbionts of nematodes (25). For the endosymbiotic bacteria, motility of the hosts might be another explanation for the lack of zonation.…”

Section: Discussionmentioning

confidence: 99%

Quantitative Molecular Analysis of the Microbial Community in Marine Arctic Sediments (Svalbard)

Ravenschlag

Sahm

Amann

2001

Appl Environ Microbiol

219

163

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Fluorescence in situ hybridization (FISH) and rRNA slot blot hybridization with 16S rRNA-targeted oligonucleotide probes were used to investigate the phylogenetic composition of a marine Arctic sediment (Svalbard). FISH resulted in the detection of a large fraction of microbes living in the top 5 cm of the sediment. Up to 65.4% ؎ 7.5% of total DAPI (4,6-diamidino-2-phenylindole) cell counts hybridized to the bacterial probe EUB338, and up to 4.9% ؎ 1.5% hybridized to the archaeal probe ARCH915. Besides ␦-proteobacterial sulfate-reducing bacteria (up to 16% 52) members of the Cytophaga-Flavobacterium cluster were the most abundant group detected in this sediment, accounting for up to 12.8% of total DAPI cell counts and up to 6.1% of prokaryotic rRNA. Furthermore, members of the order Planctomycetales accounted for up to 3.9% of total cell counts. In accordance with previous studies, these findings support the hypothesis that these bacterial groups are not simply settling with organic matter from the pelagic zone but are indigenous to the anoxic zones of marine sediments. Members of the ␥-proteobacteria also constituted a significant fraction in this sediment (6.1% ؎ 2.5% of total cell counts, 14.4% ؎ 3.6% of prokaryotic rRNA). A new probe (GAM660) specific for sequences affiliated with free-living or endosymbiotic sulfur-oxidizing bacteria was developed. A significant number of cells was detected by this probe (2.1% ؎ 0.7% of total DAPI cell counts, 13.2% ؎ 4.6% of prokaryotic rRNA), showing no clear zonation along the vertical profile. Gram-positive bacteria and the ␤-proteobacteria were near the detection limit in all sediments.Knowledge of the microbial diversity of marine pelagic and benthic communities has been greatly extended recently by molecular studies based on the analysis of 16S rDNA sequences (see, for example, references 9, 10, 20, 43, 44, 48, 50, 52, and 67). Numerous new 16S rDNA sequences have been retrieved both from marine sediments and from the water column, indicating that the vast majority of species has not been cultivated yet. Several studies using the cultivation-independent approach of 16S rDNA cloning have helped to elucidate common features within the microbial communities of specific habitats such as marine benthic environments (10,35,36,52,67). Furthermore, they have provided additional sequence information for the design and evaluation of nucleic acid probes for the identification and quantification of distinct bacterial populations.While microbial diversity can be readily studied by PCRbased 16S rDNA cloning, community structure cannot be deduced from cloning studies (3) due to potential biases introduced during DNA retrieval and amplification (17,53,65). For reliable characterization of community structure, quantitative methods such as fluorescence in situ hybridization (FISH) or rRNA slot blot hybridization are more suitable (3). To date, a number of studies have been performed using either of these two methods to quantify different groups in marine sediments (15,37,38,51,(57)(5...

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Section: Discussionmentioning

confidence: 99%

Quantitative Molecular Analysis of the Microbial Community in Marine Arctic Sediments (Svalbard)

Ravenschlag

Sahm

Amann

2001

Appl Environ Microbiol

219

163

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“…In this case, the high sulfide concentration in L. oneistus's microenvironment could still select S. majum symbionts, along with other "unwanted" microbes, off the surface of L. oneistus. In fact, symbiotic L. oneistus tolerates much higher concentrations of thiols than does S. majum (8).…”

Section: Discussionmentioning

confidence: 99%

A New C-Type Lectin Similar to the Human Immunoreceptor DC-SIGN Mediates Symbiont Acquisition by a Marine Nematode

Bulgheresi

Schabussova

Chen

et al. 2006

Appl Environ Microbiol

103

105

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Although thiotrophic symbioses have been intensively studied for the last three decades, nothing is known about the molecular mechanisms of symbiont acquisition. We used the symbiosis between the marine nematode Laxus oneistus and sulfur-oxidizing bacteria to study this process. In this association a monolayer of symbionts covers the whole cuticle of the nematode, except its anterior-most region. Here, we identify a novel Ca 2؉ -dependent mannose-specific lectin that was exclusively secreted onto the posterior, bacterium-associated region of L. oneistus cuticle. A recombinant form of this lectin induced symbiont aggregation in seawater and was able to compete with the native lectin for symbiont binding in vivo. Surprisingly, the carbohydrate recognition domain of this mannose-binding protein was similar both structurally and functionally to a human dendritic cell-specific immunoreceptor. Our results provide a molecular link between bacterial symbionts and host-secreted mucus in a marine symbiosis and suggest conservation in the mechanisms of host-microbe interactions throughout the animal kingdom.Stilbonematinae (Desmodoridae, Chromadoria) (27, 28) are especially abundant in tropical calcareous sands, where an oxidized surface layer overlies a reduced one. In the Belize Barrier Reef, two species, Laxus oneistus and Stilbonema majum, even dominate the nematode fauna of shallow sands. Stilbonematids repeatedly cross the boundary between oxidized and reduced sediment layers and thus represent an ideal substrate for bacteria that require both oxygen and sulfide. The worms, in turn, appear to obtain most of their nutrition by grazing on their symbionts (29).Another peculiar feature of symbiotic marine nematodes is a conspicuous system of glandular sensory organs (GSOs) underlying their cuticle (see Fig. 2D). The GSOs produce a mucus envelope in which symbionts may be embedded. In each GSO the secretory granules accumulate in the canal and are released onto the cuticle surface through a hollow seta (18,19).There is no evidence of vertical transmission of the symbionts, but even very small juveniles carry a complete microbial coat. Colonization of recently hatched or molted stilbonematids must be a rapid process because field collections rarely yielded nonsymbiotic stilbonematids.In L. oneistus, whose bacterial coat is composed of a single phylotype of rod-shaped ␥-Proteobacteria (26, 31, 30), symbiont recruitment must be highly selective. The microbial coat starts with a sharp onset some distance behind the anterior end, and the bacterial rods are aligned perpendicularly to the worm's surface. The absence of symbionts on the anterior region does not correlate with fewer or smaller GSOs or with reduced mucus production.Incubation in D-mannose specifically led to symbiont detachment from nematodes belonging to the genus Laxus but not from S. majum. Furthermore, this monosaccharide was found on the surface of the symbionts, but not on L. oneistus cuticle (22). These data led to the hypothesis that L. oneistus binds its s...

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“…In contrast, live observations, including the present ones, have never supported this hypothesis. Moreover, experiments have shown that small holes in an otherwise intact coat of bacteria showed no signs of closure over a period of 7 days (Hentschel et al 1999).…”

Section: Ecologymentioning

confidence: 99%

“…They live in sheltered intertidal and subtidal sulfidic sediments, mainly at the interface between the oxidized surface layer and the deeper, anoxic sediment (Ott and Novak 1989;Ott et al 1991). The symbiotic, uniform bacteria which colonize the surface of the worms in various characteristic patterns are chemoautotrophic oxidizers of sulfide and other reduced sulfur compounds (Schiemer et al 1990;Polz et al 1992Polz et al , 1994Hentschel et al 1999). The nematodes appear to graze on their symbionts (Polz et al 1992;Hoschitz et al 2001), and it has been suggested that the bacterial coat is protective against toxic hydrogen sulfide (Ott 1995;Hentschel et al 1999).…”

Section: Introductionmentioning

confidence: 99%

Leptonemella species (Desmodoridae, Stilbonematinae), benthic marine nematodes with ectosymbiotic bacteria, from littoral sand of the North Sea island of Sylt: taxonomy and ecological aspects

Riemann

Thiermann

Bock

2003

Helgoland Marine Research

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Leptonemella species represent a dominant element of the nematode fauna in sulfidic, deep sediment layers on the sandy shore of Sylt. Based on collections sampled here in 1991-1999, a taxonomic treatise is presented on the three co-existing species, Leptonemella aphanothecae Gerlach, 1950, the closely related L. vicina sp. nov., and L. gorgo Gerlach, 1950. The high incidence of pseudohermaphrodites in the material, mostly functional females with a male copulatory apparatus, is remarkable. The highest population densities of Leptonemella spp. (up to 73 individuals/10 ml sand) were found near polychaete burrows. Because of the great spatial and temporal variations in the oxygen/sulfide regime of these microhabitats, and because of the strong adhesive capabilities of Leptonemella spp., which can anchor themselves firmly to sand grains using caudal glands, we propose that a hemisessile life strategy is employed by these nematodes to fulfill the metabolic needs of their sulfide-oxidizing ectosymbionts.

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Metabolism of nitrogen and sulfur in ectosymbiotic bacteria of marine nematodes (Nematoda, Stilbonematinae)

Cited by 46 publications

References 14 publications

Quantitative Molecular Analysis of the Microbial Community in Marine Arctic Sediments (Svalbard)

Quantitative Molecular Analysis of the Microbial Community in Marine Arctic Sediments (Svalbard)

A New C-Type Lectin Similar to the Human Immunoreceptor DC-SIGN Mediates Symbiont Acquisition by a Marine Nematode

Leptonemella species (Desmodoridae, Stilbonematinae), benthic marine nematodes with ectosymbiotic bacteria, from littoral sand of the North Sea island of Sylt: taxonomy and ecological aspects

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